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BIOENERGETICS AND PHOTOSYNTHESIS

Hydrogen Production in Chlamydomonas: Photosystem II-Dependent and -Independent Pathways Differ in Their Requirement for Starch Metabolism^1,[W]

Commissariat à l'Energie Atomique, Direction des Sciences du Vivant, Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Bioénergétique et Biotechnologie des Bactéries et Microalgues, Commissariat à l'Energie Atomique Cadarache, F–13108 Saint-Paul-lez-Durance, France (V.C., A.B., D.T., S.C., L.C., G.P.); CNRS, UMR Biologie Végétale et Microbiologie Environnementale, F–13108 Saint-Paul-lez-Durance, France (V.C., A.B., D.T., S.C., L.C., G.P.); Aix Marseille Université, Laboratoire de Bioénergétique et Biotechnologie des Bactéries et Microalgues, F–13108 Saint-Paul-lez-Durance, France (V.C., A.B., D.T., S.C., L.C., G.P.); and CNRS, Unité de Glycobiologie Structurale et Fonctionnelle, UMR 8576, Université des Sciences et Technologies de Lille, F–59655 Villeneuve d'Ascq cedex, France (D.D., H.T., S.B.)

Under sulfur deprivation conditions, the green alga Chlamydomonas reinhardtii produces hydrogen in the light in a sustainable manner thanks to the contribution of two pathways, direct and indirect. In the direct pathway, photosystem II (PSII) supplies electrons to hydrogenase through the photosynthetic electron transport chain, while in the indirect pathway, hydrogen is produced in the absence of PSII through a photosystem I-dependent process. Starch metabolism has been proposed to contribute to both pathways by feeding respiration and maintaining anoxia during the direct pathway and by supplying reductants to the plastoquinone pool during the indirect pathway. At variance with this scheme, we report that a mutant lacking starch (defective for sta6) produces similar hydrogen amounts as the parental strain in conditions of sulfur deprivation. However, when PSII is inhibited by 3-(3,4-dichlorophenyl)-1,1-dimethylurea, conditions where hydrogen is produced by the indirect pathway, hydrogen production is strongly reduced in the starch-deficient mutant. We conclude that starch breakdown contributes to the indirect pathway by feeding electrons to the plastoquinone pool but is dispensable for operation of the direct pathway that prevails in the absence of DCMU. While hydrogenase induction was strongly impaired in the starch-deficient mutant under dark anaerobic conditions, wild-type-like induction was observed in the light. Because this light-driven hydrogenase induction is DCMU insensitive and strongly inhibited by carbonyl cyanide-p-trifluoromethoxyphenylhydrazone or 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, we conclude that this process is regulated by the proton gradient generated by cyclic electron flow around PSI.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Gilles Peltier (gilles.peltier{at}cea.fr).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.144576

^* Corresponding author; e-mail gilles.peltier{at}cea.fr.

Received July 10, 2009; accepted August 17, 2009; published August 21, 2009.